Ammonium metabolism in the zooxanthellate coral, stylophora pistillata

Abstract

The cycling of ammonium between the cnidarian animal host and intracellular symbiotic algae was investigated in the zooxanthellate coral Stylophora pistillata , obtained from the Gulf of Eilat. Excretion of ammonium into the surrounding water by freshly collected corals was not detectable because of efficient recycling of inorganic nitrogen between the symbionts. Excretion into surrounding water was induced by incubation in the dark, by treatment with the photosynthetic electron transport inhibitor DCMU, and by treatment with azaserine, an inhibitor of glutamine 2-oxoglutarate amido transferase (GOGAT). Methionine sulphoxamine, an inhibitor of glutamine synthetase (GS), killed the animals. The three non-lethal treatments gave similar excretion rates of 0.0112 ± 0.0011 μmol NH + 4 cm -2 h -1 . Whole coral respiration, and animal glutamate dehydrogenase (GDH) activity, which reversibly catalyses the reductive deamination of glutamate, were also measured. The ratios of GDH activity: excretion and respiration: excretion were remarkably constant, averaging 6.2 ± 1.2 mol NH + 4 mol -1 NH + 4 and 57 ± 7 mol O 2 mol -1 NH + 4 respectively. Our results suggest that GDH activity and dark respiration rates may be used to estimate quantitatively the rate of ammonium excretion in S. pistillata . From knowledge of the nitrogen content per unit area of zooxanthellae and animal tissue, the mitotic index of the algae, and the calculated excretion rate of the animal, we constructed a nitrogen budget for the coral. Our calculations suggest that recycled nitrogen accounts for 90% of the zooxanthellae nitrogen demand, and that nitrogen turns over at a rate of 0.13 per day in the algae and 0.013 per day within the animal tissue.

The function of plastids in the deep‐sea benthic foraminifer, Nonionella stella

“…In fact, blocking GOGAT activity in zooxanthellae results in NH release from corals, which suggests that the ϩ 4 role of GDH is more closely tied to respiration than to NH assimilation (Rahav et al 1989). The presence of the ϩ 4 diatom nuclear encoded enzyme nitrate reductase in N. stella supports this hypothesis.…”

“…By definition, a symbiotic relationship is mutually beneficial, as in coral-zooxanthellae symbiosis, where the algae provides reduced carbon to the host and nitrogen is recycled between the two organisms (Rahav et al 1989;Falkowski et al 1993). More than 30 yr ago, ultrastructural analysis of the marine ciliate Mesodinium rubrum revealed an ''incomplete symbiosis'' involving two enslaved organelles from different organisms: functional chloroplasts and non-ciliate mitochondria (Taylor et al 1969(Taylor et al , 1971.…”

A single-cell view of ammonium assimilation in coral–dinoflagellate symbiosis

“…The main ammonium assimilatory pathway in dinoflagellate is via the GS/GOGAT cycle (Summons and Osmond, 1981;Summons et al, 1986;Rahav et al, 1989;Roberts et al, 1999) in which GS first transfers ammonium to glutamate to produce glutamine and GOGAT then completes the cycle by catalysing the conversion of glutamine and 2-oxoglutarate to produce Glutamate (Falkowski et al, 1993;Roberts et al, 1999;Inokuchi et al, 2002). The abundance of Glutamine and Glutamate is therefore supposed to be a sensitive indicator of assimilation of nitrogen following uptake of ammonium by dinoflagellate (Flynn et al, 1994).…”

Effects of starvation, ammonium concentration, and photosynthesis on the UV-dependent accumulation of mycosporine-like amino acids (MAAs) in the coral Stylophora pistillata

“…The loss of chlorophyll a from starved corals between Days 7 and 14 (60% decline) was greater than the loss of colony protein (6% decline). Therefore, the continued increase in MAAs per cm 2 of colony surface may indicate an increase in the rate of UV-induced production of MAAs per unit chlorophyll a, perhaps as a compensation (afforded by decreased self-shading) for declining numbers of zooxanthellae and despite ongoing starvation (with ammonium derived from protein catabolism being recycled by the zooxanthellae: Rahav et al 1989). This would indicate a priority for producing UV defenses during acute exposure to UVR despite nutritional stress, although this may differ among colonies (see below).…”

“…It is perhaps not surprising that supplementing corals with ammonium has a larger effect on primary than on secondary MAAs, for it is primary MAAs that are synthesized de novo in the zooxanthellae (where most of the exogenous ammonium is assimilated: Rahav et al 1989, Grover et al 2002, and then secondarily modified in the host or its associated bacteria (Dunlap & Shick 1998, Shick 2004. In particular, it is the primary MAAs shinorine, porphyra-334, and mycosporine-2 glycine whose biosynthesis requires the addition of an amino acid (serine, threonine, and glycine, respectively) to the progenitor MAA, mycosporine-gycine.…”